Within group relationships and lack of social enhancement during object manipulation in captive Goffin’s cockatoos (Cacatua goffiniana) Within group relationships and lack of social enhancement during[.]
Learn Behav DOI 10.3758/s13420-016-0235-0 Within-group relationships and lack of social enhancement during object manipulation in captive Goffin’s cockatoos (Cacatua goffiniana) B Szabo 1,2 & T Bugnyar & A M I Auersperg # The Author(s) 2016 This article is published with open access at Springerlink.com Abstract Different types of social relationships can influence individual learning strategies in structured groups of animals Studies on a number of avian species have suggested that local and/or stimulus enhancement are important ingredients of the respective species’ exploration modes Our aim was to identify the role of enhancement during object manipulation in different social contexts We used focal observations to identify a linear dominance hierarchy as well as affiliative relationships between individuals in a group of 14 Goffin’s cockatoos (Cacatua goffiniana, formerly goffini) Thereafter, in an unrewarded object choice task, several pairs of subjects were tested for a possible influence of social enhancement (local vs stimulus) in three conditions: dominance, affiliation, and kinship Our results suggest strong individual biases Whereas previous studies on ravens and kea had indicated that enhancement in a non-food-related task was influenced by the social relationship between a demonstrator and an observer (affiliated – nonaffiliated), we found no such effects in our study group In this context, Goffin’s cockatoos’ object learning seems to take Electronic supplementary material The online version of this article (doi:10.3758/s13420-016-0235-0) contains supplementary material, which is available to authorized users * B Szabo birgit.szabo@gmx.at Department of Biological Sciences, Macquarie University, 209 Culloden Road, Building W19A, Marsfield, NSW 2122, Australia Department of Cognitive Biology, University of Vienna, Althanstr 14, Vienna 1090, Austria Comparative Cognition Unit, Messerli Research Institute, University of Veterinary Medicine, Medical University of Vienna, University of Vienna, Veterinärplatz 1, Vienna 1210, Austria place more on an individual level, despite their generally high motivation to manipulate nonfood items Keywords Avian cognition Social learning Parrot Dominance hierarchy To regulate access to resources and mates (Ficken, Weise, & Popp, 1990; Hinde, 1976), many group-living animals develop dominance hierarchies (Ficken et al., 1990; Hinde, 1976; Humphrey, 1976) The hierarchical position is usually established by a repeated exchange of agonistic interactions (Drews, 1993; Kappeler, 2006; Paz-y-Mino et al 2004), or is even inherited from the parents (Bergstrom & Fedigan, 2010) or transferred from mating partners (Lorenz, 1935; Röell, 1978) In addition to agonistic interactions, social groups can also be characterized by affiliative relationships between both related and unrelated individuals (e.g., Hinde, 1976) Affiliates spend more time in close proximity and tend to show high levels of reciprocal socio-positive behaviors (Bonnie & de Waal, 2006; Schwab, Bugnyar, Schloegl, & Kotrschal, 2008) Individuals profit from such relationships by gaining support in agonistic interactions, sharing valuable information or resources (Fraser & Bugnyar, 2010), and in the case of kin, may increase their inclusive fitness (Hamilton, 1964a, 1964b) Keeping track of the identities and social relationships of all members within a social group and adjusting behavioral responses accordingly may represent a high cognitive load to some species (see the summaries in Byrne, 1989; Humphrey, 1976) During interactions, information may be transferred from one individual to another, a process called social learning (Heyes, 1994) Social learning is considered advantageous particularly in uncertain situations, when an individual is confronted with unfamiliar food or predators (Laland, 2004; Zentall, 2012) In frequently changing environments, Learn Behav however, social learning can lead to misinformation, since any advantageous information may quickly be outdated (Giraldeau et al., 2002; Kendal, Coolen, & Laland, 2009a) Hence, to be adaptive, social learning should be used selectively (Galef, 1995); that is, when individually sampling the environment bears high temporal and energy costs and/or a high risk of injury (Bonnie & Earley, 2007; Giraldeau et al., 2002; Kendal et al., 2009a; Kendal, Giraldeau, & Laland, 2009b), individuals should revert to learning from conspecifics (Arbilly, Weissman, Feldman, & Grodzinski, 2014; Boyd & Richerson, 1988; Galef, 1995; Giraldeau, Valone, & Templeton, 2002; Kendal, Coolen, van Bergen, & Laland, 2005; Laland, 2004; Zentall, 2012) It is well-known that humans behave according to the norms dictated by their social environment (Merton & Rossi, 1949, cited by Bearden & Etzel, 1982) The phenomenon that humans are influenced by the decisions and opinions of others (Bandura, 1986) is used by marketers for designing advertisements (Bearden & Etzel, 1982) Coussi-Korbel and Fragaszy (1995) proposed a similar influence in animals—namely, that the behavior patterns of one individual will have an influence on others, depending on their relationship (Katzir, 1982; Stöwe et al., 2006), and should alter their decisions with respect to the identity of a demonstrator during social learning Expanding on this line of thought, Laland (2004) and Rendell et al (2011) described a number of strategies concerning when social learning occurs and from whom individuals should learn On the basis of the type of information gained from the observation of a demonstrator (e.g., single stimulus, location, stimulus–stimulus relationship, affordances, or complex motor tasks), social learning is divided into subcategories Among these, stimulus and local enhancement are assumed to be two of its simplest but most widespread forms (Coussi-Korbel & Fragaszy, 1995; Hoppitt & Laland, 2008) According to Hoppitt and Laland, stimulus enhancement occurs when the observation of a demonstrator (or its products) exposes the observer to a single stimulus at a time t1 and that single stimulus exposure effects a change in that observer’s behavior, at a second time t2 In contrast, local enhancement occurs when, after or during a demonstrator’s presence at, or interaction with objects at, a particular location, an observer is more likely to visit or interact with objects at that location (Hoppitt & Laland, 2008) In accordance with these definitions, an increase in stimulus handling time can be predicted if enhancement occurs By allowing frequent and stable physical proximity and/or by directing a conspecific’s attention to specific stimuli, social dynamics could favor different forms of social learning (CoussiKorbel & Fragaszy, 1995) Only a small number of studies have focused on the influence of these dynamics on different types of enhancement, and even fewer have done so in a nonfeeding context Although enhancement may occur in both feeding and nonfeeding situations, independent of the benefits, a lack of enhancement in one context might not necessarily indicate a lack thereof in the other, or a general lack of the ability to use any form of social learning The results of previous studies in birds have demonstrated a surprising variety of social influence on enhancement in three corvids (Corvus corax: Schwab, Bugnyar & Kotrschal 2008a; Heyse, 2012; Corvus corone corone & C c cornix: Miller, Schiestl, Whiten, Schwab, & Bugnyar, 2014; Corvus monedula: Schwab, Bugnyar, & Kotrschal, 2008), as well as in New Zealand’s kea parrots (Nestor notabilis: Heyse, 2012; see Table 1) Stimulus enhancement was demonstrated by Schwab, Bugnyar, Schloegl, and Kotrschal (2008) in sibling and nonsibling pairs of juvenile ravens First, subjects watched a demonstrator manipulate a nonfood object in an adjacent room Thereafter, the observer was confronted with a set of five objects, including the target object that the demonstrator had manipulated just moments before Subjects within sibling pairs manipulated the target object significantly longer than the other four objects, whereas nonrelated birds showed no enhancement Using the same paradigm, Schwab, Bugnyar, and Kotrschal (2008) showed that juvenile jackdaws were influenced by neither a sibling’s nor a nonsibling’s choice However, two additional food-related experiments demonstrated enhancement in juvenile and adult jackdaws observing nonsiblings/nonpair mates feeding from one of two distinctively colored boxes containing mealworms Controls for side preferences indicated that the mechanism was stimulus rather than local enhancement These results suggest an impact of species’ feeding ecology on enhancement Ravens use food caching and develop cache protection or pilfering strategies during social object play and play-caching (Bugnyar et al 2007) Noncaching corvids such as jackdaws may, therefore, be less attentive to the (nonfood) object manipulations of others On the basis of these findings, food seems to have greater influence on noncaching corvids Miller et al (2014) studied social enhancement in freeranging carrion crows by providing groups of crows with two pairs of objects Observers were more likely to interact with an object at the same location as a demonstrator than with a second, identical object m away In half of the sessions, a piece of bread was placed underneath the objects The authors state that co-feeding occurred more often than affiliative and agonistic behaviors and that the animals were very tolerant of conspecifics feeding next to them It is therefore not surprising that local enhancement was detected, since tolerating conspecifics in close proximity is a necessary prerequisite (CoussiKorbel & Fragaszy, 1995) Another study using a group setup tested social enhancement in ravens and kea (Heyse, 2012) Subjects were presented with four pairs of items, among which they could choose freely Generally, both species showed stimulus enhancement most frequently, and it was favored by affiliated subjects Additionally, higher-ranking ravens showed more local enhancement Rank-dependent resource access might have C c corone 115 juvenile/ adult Current study Heyse (2012) 11 juvenile/ adult Nestor notabilis Cackatua 14 juvenile/ goffiniana adult 11 juvenile/ adult C corax Schwab, Bugnyar, Corvus 12 juvenile Schloegl, & Kotrschal corax (2008) Miller et al (2014) C c cornix 115 juvenile/ adult Corvus 20 juvenile monedula Corvus 20 juvenile/ monedula adult Subject Age Schwab, Bugnyar, & Kotrschal (2008) N Species Study pairs pairs pairs pairs pairs pairs repeatedly repeatedly partly familiar once by observer unfamiliar unfamiliar repeatedly familiar pairs pairs repeatedly familiar no no no partly partly no once by pair yes familiar once by observer once by pair no unfamiliar Object Familiarity unfamiliar Test Food InvolveObject Use ment one object objects including (=target) target distinctly distinctly colored colored boxes boxes one object objects (=target) including target pairs pairs Demonstration Presentation of Objects grouped by limited dissimilarity, target identical pair of same size & shape, different color pair of same size & shape, different color objects in a pair of different complexity, pairs identical objects in a pair of different complexity, pairs identical first & third similar, second & fourth similar, not identical grouped by shape/ size, target identical grouped by color, identical Object Appearance physical contact physical contact physical contact no contact physical contact physical contact visual contact physical contact no contact no contact no contact Test physical contact physical contact visual contact visual contact visual contact Demonstration Contact yes possible possible possible possible yes yes yes Role Switch possible possible possible possible possible possible possible possible Experimenter Induced Enhancement Table Comparative summary of the methodologies used within the presented sample of avian literature testing for social enhancement: Study, species, sample size, age of subjects., presentation of objects during the demonstration and the test phase, the subjects prior familiarity with the used objects, type of object presentation, food/no-food involved, the appearance of the introduced objects, the type of contact between the demonstrator and the subject during the demonstration and the test phase, if demonstrators participated as subjects during the study and vice versa and if the arrangement of the setup was observable to the subjects Learn Behav Learn Behav enabled them to use local enhancement as a learning mechanism (Laland, 2004), whereas affiliation could lead to an increased awareness of a conspecific’s actions, and attention might selectively be directed to specific stimuli, making stimulus enhancement a likely learning mechanism (CoussiKorbel & Fragaszy, 1995) Goffin’s cockatoos (Cacatua goffiniana; formerly goffini) are generalist parrots endemic to the Tanimbar Islands in Indonesia They live in social groups (N < 100), mated pairs, or family groups in tropical dry forests (Cahyadin, Jepson, & Manoppo, 1994; Jepson, Brickle, & Chayadin, 2001) In captivity, these cockatoos show a wide range of social interactions, as well as complex and structured object play and manipulative exploration behavior (Auersperg, Oswald, et al 2014; Auersperg et al., 2015) Behavioral observations have revealed that they spend most of the day manipulating a variety of different objects (Auersperg et al., 2015; Szabo, 2013) and, on the basis of these findings, we decided to apply an unrewarded object choice task to study enhancement Furthermore, this species had previously demonstrated high levels of performance in a number of cognitive tasks, such as impulse control (Auersperg, Laumer, et al 2012), sequential problem solving (Auersperg, Kacelnik, & von Bayern, 2013), Piagetian object permanence (Auersperg, Szabo, von Bayern, & Bugnyar, 2014), and the capacity to innovate tool use as a solution to a novel problem (Auersperg, Szabo, von Bayern, & Kacelnik, 2012) Notably, Goffin’s cockatoos are able to socially transmit information to conspecifics in a foraging task involving the use of tools (Auersperg, von Bayern, et al., 2014) Enhancement therefore seems to play a role in at least some foraging tasks (Auersperg, von Bayern, et al., 2014); it is, however, unclear which enhancement processes (local vs stimulus) are common, and to what extent enhancement is influenced by their social relationship to the respective demonstrators On the basis of our current state of knowledge, the Goffin is an opportunist/generalist species that explores a wide range of visually distinct resources (unpublished field data); therefore, stimulus enhancement seems most likely as an enhancement mechanism Furthermore, like many other Cacatua species, they show high levels of aggression toward nonaffiliated individuals (Forshaw & Cooper, 2003) To avoid aggression, attention might be directed selectively toward affiliates and subordinates, rather than dominant conspecifics However, the opposite might be the case, because dominant individuals generally have better access to desired or limited resources, and are therefore a more reliable source of information (Laland, 2004) Gaining a more detailed insight into how social relationships influence their object exploration would represent an important next step to improve our understanding of the role of social learning in the technical abilities of this avian model Our aim was first to determine the social structure of our available group, by evaluating the type of dominance hierarchy as well as possible affiliative relationships between individuals, and to create pairs in three relationship categories (determined by rank, unrelated affiliation and relatedness) Thereafter, we applied a simple social-learning experiment testing for enhancement in a non-food-related object choice task Method Subjects and housing Fourteen subadult–adult (20 months to years of age at the time of the study) Goffin’s cockatoos (Cacatua goffiniana; formerly goffini), seven males and seven females, participated in this study All of the birds were hand-reared by accredited German breeders and purchased with documentary evidence of origin and CITES papers For individual identification, they were marked by colored leg bands Previously, the whole group had participated in a number of cognitive experiments (see above) The animals are housed together as a social group in an aviary consisting of an indoor part (45-m2 ground space, 3– m high, wall to gable) and an outdoor part (150-m2 ground space, 3–4.5 m high) The indoor part is enriched with wooden, free-hanging perches, artificial ponds, and wooden chew toys; the outdoor part is equipped with wooden, free-hanging perches and trees During winter—October to May—the aviary is kept at 20 °C Fresh drinking water and basic food (Australian Parrot Loro Parque Mix mixed with dried fruits) are available ad libitum, supplemented by two to three types of fresh fruit and various protein sources in the morning The described housing conditions comply with the Austrian Federal Act on the Protection of Animals, and importantly, since this study was strictly noninvasive and based purely on behavioral tests, it was not classified as an animal experiment under the Austrian Animal Experiments Act Behavioral monitoring To record affiliative and agonistic behaviors, we conducted two cycles of behavioral observations, once a day between am and pm We observed the group from outside the outdoor aviary four days a week during the summer (June to September 2012) and from outside the indoor aviary once a week during the winter (November 2012 to February 2013) Observations consisted of a 10-min focal per individual, throughout which time we recorded allopreening incidents and all displacements that occurred (see Table 2) Between every two focals, the nearest neighbor of each individual was documented BNearest neighbor^ was defined as two or more individuals being within a range of 40 cm of one another Learn Behav Table List of social behaviors used to calculate the hierarchy and affiliations (affiliative behaviors that occurred